Co-adaptation is key to coexisting with large carnivores

Science & Society

Co-Adaptation Is Key to Coexisting with Large

Carnivores

Neil H. Carter

* and John D.C. Linnell

There is a pressing need to inte- grate large carnivore species into multi-uselandscapesoutsidepro- tectedareas.However, anunclear understandingofcoexistencehin- ders the realization of this goal.

Here,weprovideacomprehensive conceptualization of coexistence in which mutual adaptations by bothlargecarnivoresandhumans havea centralrole.

CoexistenceandGlobal CarnivoreRecovery

Protectedareasarecrucialtolargecarni- vore conservation. However, the vast ranges required by these animals mean thatco-occurrencewith humansis, and hasbeen,commoninsharedlandscapes outsideprotectedareas(Figure1).Given thatsharedlandscapesoftenrepresenta vital part of their remaining geographic distribution[15],eradicationoflargecar- nivorespeciesfromtheseareasthreatens theirconservation.Despitethis,theneed for conservation of large carnivores in proximitytohumanpopulationsoftengen- eratesintensedebate,withakeypointof contention being whether, and to what degree, the negative impacts humans andlargecarnivoreshaveoneachother canbesufficientlyminimized.Thus,oper- ationalizinghuman–carnivorecoexistence insharedlandscapesisessentialtoglobal carnivorerecoveryeffortsandmaintaining (orimproving)humanwellbeing[1–3].Yet, aclearunderstandingofwhatcoexistence meansis lackingdespiteitswide use in both popular and scientific literature. In

part,thisisbecausecoexistencecanbe interpreted very differently when viewed fromeitherasocialornaturalscienceper- spective. An unclear, inconsistent, or naïve conceptualization of coexistence hinderstheabilityofopposingstakeholder groupstoengageindialogandprecludes themuch-neededdevelopmentofstrong andcomparableefficacycriteriafordiffer- entcoexistencestrategies.

AComprehensiveConcept of Coexistence

Based on our combined experience of working on largecarnivore conservation issues,weconceptualizecoexistenceasa

‘dynamic but sustainable state in which humans and large carnivores co-adapt to living in shared landscapes where human interactions with carnivores are governed by effective institutions that ensure long-term carnivore population persistence,sociallegitimacy,andtolera- blelevelsofrisk’.Ourconceptofcoexis- tenceincludesbothhuman–carnivoreand human–human interactions, helping to unify disparate interpretations of coexis- tence from different disciplines. Indeed, coexistence emerges from the interac- tionswithincoupledsocioecologicalsys- tems, in which the human and natural systems are fundamentally integrated [3]. Specifically, mutual adaptations between humans and large carnivores are key mechanisms facilitating coexis- tenceinspaceandtime.Flexibleinstitu- tions (i.e., the formal and informal rules that govern human behavior) have an essentialroleinfosteringhuman adapta- tiontocarnivores. Althoughourconcept ofcoexistencemightbedifficulttoachieve inreality,itcanserveasabenchmarkto strive towards. Here, we highlight key topics informing our concept of coexistence.

CoexistenceandRisksfrom Carnivores

Coexistencedoesnotprecluderisksfrom carnivores;rather,it necessitateshuman toleranceoftheserisksandbringingrisks to tolerable levels. The most common

risksfromcarnivoresarethoseassociated with damage caused bydepredation on livestock, competition with hunters, and attacks on humans. These risks are thoughttodirectlyleadtointolerantbehav- iors by humans, such as illegal killing of carnivores,whichcanjeopardizecarnivore recoveryefforts[4].Managershaveaccess to several technical solutions to mitigate carnivore-related risks; however, recent studies have demonstrated that human tolerance of carnivores is sometimes stronglyrelated to social,cultural,cogni- tive,andemotionalfactors,andnotonlyto the economic and material interactions withcarnivoresperse[4].Despitelivestock depredationsbysnowleopards(Panthera uncia), for example, Tibetan Buddhist monasteries protectsnow leopards and their habitatsincertainareasbecauseof theirsignificantculturalandreligiousvalues [5].Furthermore,therecentcomebackof large carnivore species to regions ofthe USAandEuropeafterbeingnearlyeradi- cated [1,2] indicates that changes in humantolerancetocarnivores(e.g.,oper- ationalizedintheformofpublicsupportfor moreprotectivepolicies)haveimplications onlong-termcarnivorepersistence.Given thatevidenceindicatesthatthelong-term viability of large carnivore populations in shared landscapes is related to human tolerance,learningmoreabouthumantol- erancetocarnivoresisanimportantfuture researchactivity.

ConflictingPriorities,Governance, andCoexistence

Coexistence is influenced not only by human–carnivore interactions, but also human–human interactions that affect carnivores[6].Avarietyofhumanattitudes towardcarnivoresandtheirconservation simultaneously exist among humans within and across regions and cultures.

This pluralityinattitudescangiveriseto multipleandconflictingprioritiesandgoals regarding the presence of carnivores in shared landscapes. For example, the international community might endorse policies promoting more carnivores in multi-use landscapes, whereas local

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communitiesmightnotbewillingtoshare theirlandscapeswithcarnivoresbecause oftheriskstohumanlivelihoodandsafety.

Failuretoaddressthedisparityinhuman norms, attitudes, and knowledge about carnivoresamongdifferenthumangroups canunderminecoexistence.Forexample, conflictsbetweenstakeholdergroupsand reducedtrustintheauthoritiesinpartsof Scandinavia are thought to be major causesofillegalkillingoflargecarnivores [7].OnestudyinSwedenfoundthatillegal killingofwolves (Canislupus)accounted

forapproximatelyhalfofthetotalmortality ofthewolfpopulation[8].

Avarietyofmeasuresexisttoreducethe impactsonhumansofhavinglargecarni- voresinsharedlandscapes,rangingfrom economic compensation and incentives, informationcampaigns,spatialzoning(e.

g.,habitatprotectionfromhumandevel- opment), technical changes to livestock husbandry, the restoration of wild prey populations,andallowinglimitedhunting oflargecarnivores,amongothers.While

these measurescanbeuseful,ourcon- cept of coexistence suggests that they should be supplemented with interven- tionsthataddressthehumanandethical facets more directly, such as efforts to engagediversestakeholdergroups,build trust and dialog between groups of humanswith differentviewpoints toward carnivores,ortheadoptionofnoveldeci- sion-makingstructuresthatensurepartic- ipation and legitimacy. For example, participatory processes, characterized by bottom-up representation and

Spoed Hyena

Crocuta crocuta Ethiopia: high densies in agricultural and peri-urban environments

Asiac Black Bear

Ursus thibetanus Japan: on Honshu; living in managed forests and mixed forest-farmland landscapes in the immediate proximity of very large urban areas

JaguarPanthera onca Mexico: persistence in community-managed forests Brazil: persistence in transformed landscapes given the maintenance of certain degrees of forest cover

Asiac Lion Panthera leo India: expansion of populaon from its refuge in the Gir forest to the surrounding farmlands, pastoral lands, and mul-use forests

Snow Leopard

Panthera unica Central Asia: current distribuon is mostly outside protected areas in habitats used for producon of livestock, small-scale agriculture, and hunng

Tiger Panthera gris Nepal: resident in mul-use buffer zones around Chitwan Naonal Park India: occurring in mul-use landscapes connecng protected areas in central landscapes

Leopard Panthera pardus India: high densies in human-dominated agricultural landscapes, despite lack of forest and wild prey. Long-term persistence in Sanjay Gandhi Naonal Park, city of Mumbai

Brown Bear Ursus arctos Europe: occupying mul-use forests that are used for mber producon, hunng, recreaon, and livestock grazing

African Lion Panthera leo Kenya: occur in many mul-use areas, especially those used for livestock producon. Have begun to occupy peri-urban areas around the city of Nairobi

Cheetah Acionyx jubatus Namibia: large populaons found living in ranchlands

Puma Puma concolor

Midwestern region, USA:

Increasingly found in recent decades throughout the Midwestern USA California: persistence in close proximity to heavily populated urban areas

Brazil: inhabit areas dominated by plantaon forests

Wolf Canis lupus

Great Lakes region, USA:

increasingly found in fragmented forest–farmland mosaic landscapes of Michigan, Minnesota, and Wisconsin Europe: occupying some intensively farmed croplands and forest-farmland mosaics

Coyote Canis latrans USA: now occupy the urban areas of many North American cies, such as Chicago and Detroit

American Black Bear

Ursus americanus Eastern USA: commonly found in farmlands and suburban areas

Figure1.ExamplesofLargeCarnivoreSpeciesthatInhabit(eitherPersistingorRecovering)Multi-UseLandscapesoutsideProtectedAreas.These examplesarenonexhaustivebutillustratethefactthatarangeofcarnivorespeciesarecurrentlysharinglandscapeswithhumansaroundtheworld.Negativeeffectsand conflictsassociatedwiththesecarnivoresvarygreatlyineachoftheselandscapes,butcansometimesbesevere.Theimportanceofsharedlandscapesforglobal carnivorerecoveryeffortsnecessitatesamoreholistic conceptualizationofhuman–carnivorecoexistencethatcanbeoperationalized ontheground.Seethe supplementalinformationonlineforreferences.PhotosreproducedcourtesyofEmmanuelKellerviaFlickr/CreativeCommons.

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legitimization, haveproven successfulat negotiatingoutcomesthatareviewedas acceptable, especially if some form of upward and downward accountability exists [9]. Such interventions have the potential to address issues of scale in governance. For example, overall goals ofcarnivoreconservationinsharedland- scapescanbedefinedatasupernational ornationalscale,whilelocalcommunities canadoptmorespecific,locallyadapted policiesandpracticesthatareconstrained bythosebroader-scale goalsandlimita- tions.Inshort,awiderarray ofinterven- tions, suchas, those mentioned above, canencouragecoexistencebyimproving institutional fit; that is, the alignment of institutionsand carnivore-occupied eco- systems,andbetweensetsofstakehold- ers[10].

CoexistencethroughCo- Adaptation

Giventhecomplexanddynamicnatureof human–carnivore interactions, we con- tend that mutual adaptations between humans and carnivores in shared land- scapesarecrucialtoachievingandmain- taining coexistence. Instead of a purely evolution-based denotation, adaptation inthis context means thathumans and carnivoresareabletochangetheirbehav- ior, learn from experience, and pursue their owninterests with respectto each other. Humans and carnivores have adaptedthustoeachotherformillennia;

for example, carnivores feeding on domestic livestock or humans lethally removingcarnivorestoreducerisks.How- ever,interms of facilitatingcoexistence, we are concerned with mutual adapta- tions that result in minimal negative impacts of humans and carnivores on each other(carnivore impact on human livelihoodandsafety,andhumanimpact oncarnivorepopulationpersistence).

Recentstudieshave documentedasur- prisingabilityoflargecarnivorestoadapt tohumans.Forexample,cougars(Puma concolor) navigate through areas in

California with high human densities by usingriparianwoodlands[11].Wilddogs (Lycaonpictus)livingoncommunitylands outside protected areas were found to maintainenergyrequirementsbyshifting their diet to smaller wild prey species insteadoffeedingonlivestock[12].Tigers spatiallyoverlappedwithlargenumbersof localhumanscollectingnaturalresources from forestsinside andoutside Chitwan NationalPark,Nepal[13].Spatialoverlap did not always lead to encounters between tigers and humans because the latter were most active during the dayandtigersatnight.Thiswasalsoseen withtheleopards(Pantherapardus)shar- ing space with humans in Maharashtra, India[14].Theseexamplesareencourag- ingsignsthatlargecarnivorescanadapt to humansonshared landscapes;how- ever,moreresearchisneededtoassess howsuchadaptations affectlargecarni- vore population viability as wellas large carnivoreregulationofprey,smallercarni- vores,andecosystems.

Although some large carnivore species canadapttohuman-modifiedlandscapes given sufficient prey and habitat, this capacity can increase the likelihood of negative encounters between humans andcarnivores.Humanresponsetoneg- ativeencounterswithlargecarnivoreshas oftenentailed the reduction ofcarnivore numbersthroughlethalmethods,suchas poisons.However,duringhumanity'slong historyofinteractingwith carnivores, we have also learned to adapt to carnivore presence,minimizingtheneedtoreduce their populationsizes.Examplesofsuch human adaptation to carnivores include the use of livestock-guarding dogs, bomas, and nonlethal repellents (e.g., placinglightsoverlivestockcorrals).Other examplesincludeavoidingpotentiallyrisky situations by understanding carnivore behavior(e.g., notjoggingwith adogin cougarterritory),reducingtheamountof human-producedfoodaccessibletocar- nivores (e.g., through bear-proof trash bins or by disposing of livestock

carcassesawayfromhumansettlements), orhavingadultsherdlivestockratherthan children.Anunwillingness(e.g.,duetorisk intolerance)orinability(e.g.,duetolackof resourcesorknowledge)ofindividualsto behaviorallyadapttothepresenceofcar- nivoresonshared landscapesare major challenges to coexistence, because not doingsoismorelikelytoaggravatecon- flict.Therefore,overcomingthesehurdles mightrelyonlocalcommunityleadersto endorse behavioral adaptations or con- servationorganizationstoimplementvari- ous programs,suchassocial marketing campaigns.Moreover,institutionstasked with ensuring that the benefits (tangible and intangible) of large carnivores are available to current and future citizens can incentivize (e.g., performance pay- ments)andregulate(e.g.,enforcingsoci- etal mandates) human adaptations to largecarnivores.

Concluding Remarks

Manyquestionsremainabouthowtoeval- uate andoperationalize coexistence.For example, whatspatialscaleismostrele- vant(e.g.,supernational,national,orsub- national)fordifferentcontextsandinwhich casesiscoexistencemorestronglyrelated tothebehaviorsandhabitatconditionsof large carnivoresortogovernanceinstitu- tionsandhumanrisktolerances?Thecon- ceptofcoexistencepresentedherecanbe a starting point from which to advance boththeinterdisciplinarytheoryandprac- tice ofcoexistence,which isincreasingly urgentinanevermorehuman-dominated world.Firststepsshouldcomprisestudies fromarangeofculturaland/orinstitutional settings,and fromabroadrangeofspe- cies other than carnivores, such as wild herbivores, to identify factorspromoting, and inhibiting, sustainable interactions between humans and wildlife ingeneral.

Insightsfromsuchstudiescanhelprecon- ciledebatesaboutwildlifeconservationin sharedlandscapesand advancebroader discoursesinconservation,suchasthose related to rewilding, novel ecosystems, andland-sharingversusland-sparing.

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Acknowledgments

ThisworkbenefitedfromsupportfromtheNational Socio-EnvironmentalSynthesisCenter(SESYNC)– NSF award DBI-1052875, NSF Idaho EPSCoR Program, NSF Award IIA-1301792, and the Research CouncilofNorway. Theauthorswould liketothankoneanonymousreviewerfortheirhelp- fulcomments.

SupplementalInformation

Supplementalinformationassociatedwiththisarticle canbefound,intheonlineversion,athttp://dx.doi.

org/10.1016/j.tree.2016.05.006.

1BoiseStateUniversity,Human-EnvironmentSystems Center,Boise,ID,USA

2NorwegianInstituteforNatureResearch,Trondheim, Norway

*Correspondence:neilcarter@boisestate.edu(N.H.Carter).

http://dx.doi.org/10.1016/j.tree.2016.05.006

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Science & Society

Coexistence with Large Carnivores Informed by

Community Ecology

Guillaume Chapron

* and José Vicente López-Bao

Conserving predators on an increasinglycrowdedplanetbrings verydifficult challenges.Here, we argue that community ecology theory can help conserve these speciesinhuman-dominatedland- scapes.Lettinghumansandpred- atorssharethesamelandscapesis similartomaintainingacommunity ofpredatoryspecies,oneofwhich ishumans.

Biodiversityis facing a majorcrisisand conservationeffortsarefailingtoreverse the 6th mass extinction caused by the increasingly destructive impact of humans on the biosphere [1]. Species such as large-bodied predators at the topsoffoodchainsbringadditionalcon- servationchallenges,raisingthequestion of whether these species will survive the 21st century [2]. Large carnivores haveparticularecologicalcharacteristics, such as low densities, large home ranges,orlimitedreproductivepotential, that require their conservation to be plannedaccordinglyatalandscapelevel [3]. In addition, large carnivores fre- quently enterinto conflict with humans by competing for game, predating live- stock and pets, or threatening public safety. Asaresult,due mainlytodirect persecutionandhabitatloss,mostlarge carnivores are experiencing a dramatic declineglobally intheirpopulationsand ranges[2].Manylargecarnivorespecies areatriskofextinction[2]andarguably the most charismatic of all large carni- vores, the lion (Panthera leo), is now

extinct in most parts of Africa and is threatened in its remaining strongholds [4]. Still, concurrent with this global decline,onecontinentisseeinganunex- pectedlarge-scalerecoveryofitsprevi- ously lost large carnivore populations.

Despite being densely populated (ca.

100 inhabitants/km²)and having few, if any, areas free from human activities, Europetodayhostsgrowingpopulations ofbears(Ursusarctos),lynx(Lynxlynx), and wolves (Canis lupus), accounting for more than 40000 individuals alto- gether [5]. Interestingly, mostEuropean countries, despite being culturally, economically, and politically diverse, shareacommonapproachtolargecar- nivoreconservation:theyallowlargecar- nivoresand humanstosharethe same landscape, or at least do not actively prevent them from doing soon alarge scale.

We term this conservation approach

‘coexistence’anddefineit asthelasting persistenceofself-sustaininglargecarni- vore populations in human-dominated landscapes.Insuchlandscapes,wepro- pose that coexistence is similar to the maintenanceofacommunityofpredatory speciescomprising largecarnivoresand humans. Ecologists have shown that communities of competing species will converge to single-species communities when one speciesdisplaysstrongcom- petitiveabilitiesandhaslimitednichedif- ferentiationfromtheotherspecies[6].By contrast, speciescancoexistwhen they show moderatecompetitive abilities and largeniche differentiation.Weargue that conservinglargecarnivoresintheAnthro- poceneisaquestionrelevantforcommu- nity ecology: can a hyperpredator (humans)[7]avoiddisplacingothercom- peting predatory species (large carni- vores) by becoming less competitive andadoptinghighernichedifferentiation?

Inthecontextofcoexistence,thecompet- itiveabilityofhumansreferstotheover- exploitation of large carnivores and destruction of their habitats. Human

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